J. Nannoplankton Res., 38(1), 2020, pp. 41–47 © 2020 International Nannoplankton Association
ISSN 1210-8049 Printed by The Sheridan Press, USA

41

Verification of the life-cycle of Helicosphaera pavimentum,
and discussion of the identity of Syracolithus dalmaticus
Jeremy R. Young

Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK; jeremy.young@ucl.ac.uk

Jasna Arapov, Sanda Skejić, Ana Bakrač, Mia Bužančić

Institute of Oceanography and Fisheries, Šetalište I. Meštrovića 63, 21000 Split, Croatia; arapov@izor.hr, sandor@izor.hr

Maria V. Triantaphyllou

Faculty of Geology and Geoenvironment, National and Kapodistrian University of Athens, Panepistimioupolis 15784, Athens, Greece;
mtriant@geol.uoa.gr
Manuscript received 30th March, 2019; revised manuscript accepted 16th March, 2020

Abstract A new observation of a combination coccosphere of Helicosphaera pavimentum and Syracolithus dalmaticus confirms the previous tentative suggestion of Triantaphyllou et al. (2016) that these are alternate life-cycle
phases of a single species. A re-examination of the type description of S. dalmaticus, however, showed that the namehas been misapplied, and that the holococcolith phase of the life-cycle of H. pavimentum has never been described.
Hence, the correct name for the species remains H. pavimentum. It is further argued that both S. dalmaticus and Homozygosphaera vercellii are synonyms of the holococcolith phase of Coronosphaera mediterranea––C. mediterranea
HOL wettsteinii type. This further means that Coronosphaera is a junior synonym of not only Zygosphaera, but also
Syracolithus. As such, we definitively accept the conclusion of Triantaphyllou et al. (2016) that the genus Coronosphaera should be recombined into Syracosphaera.
Keywords life-cycle, Helicosphaera, taxonomy, Syracolithus
1. Introduction
Combination coccospheres are invaluable in providing
data on the life-cycles of coccolithophores and so provide
fundamental data on their biology (e.g. Cros et al., 2000;
Geisen et al., 2002). Each individual life-cycle association that is established in this way is a valuable contribution to understanding coccolithophore biology. However,such associations can also cause taxonomic complications. Whenever a new association is established between
a pair of coccosphere types that were previously treated as
separate species, but are now known to represent alternate
life-cycle stages, the nomenclatural taxonomy needs to bereviewed. It is necessary to determine which is the correct name for the species, which name is a junior synonym
and whether there are any further taxonomic implications.
For the most part, taxonomic interpretations have been
relatively straightforward, but there has always been thepossibility of a more complex case. We present here newobservations that confirm a long-suspected life-cycle association, and discuss the somewhat complex taxonomic
issues that have arisen from it.
Our new observations primarily deal with a distinctive, small species of Helicosphaera––H. pavimentum.
The only previous evidence for its life-cycle association

was a single possible combination coccosphere with Syracolithus dalmaticus that was reported by Triantaphyllou etal. (2016). The other Helicosphaera species (H. carteri, H.
wallichii and H. hyalina) are, however, well established as
forming distinctive holococcoliths, which were formerly
placed in the genus Syracolithus, although it is still not
clear which holococcolith morphologies are associatedwith each heterococcolith-based species (Cros et al., 2000;
Geisen et al., 2002; Couapel et al., 2009; Young & Bown,2014).
2. Material and methods
A sea-water sample was collected at Station Stončica on
27 March, 2018, at 0 m depth (43.0000˚N, 16.3333˚E;
maximum station depth 103 m). The sample of 500 ml was
taken with a Nansen bottle (1.7 litres) and fixed with neutralised formalin at a final concentration of 2%. For scanning electron microscope (SEM) analysis, a subsample of

100 ml was filtered using a 13-mm-diameter Whatman
polycarbonate filter, with a pore size of 1 µm. The filter
was dried in a desiccator for 24 hours and, afterwards, wasmounted on an aluminium stub, coated with gold (Quorum
Q150R ES) and analysed at a magnification of x2500 using a Tescan MIRA 3 SEM. The coccosphere abundance

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Young, Arapov, Skejić, Bakrač, Bužančić, Triantaphyllou

was calculated following Bollmann et al. (2002). A totalof 115 coccospheres were determined from 374 analysed
fields.
Values of the supporting environmental parameters,
including temperature (T), salinity (S), oxygen saturation(O2), alkalinity (pH), nitrates (NO3–), nitrites (NO2–), ammonium (NH4+), total inorganic nitrogen (TIN), organic
nitrogen (NORG), phosphates (PO43–), organic phosphorus (PORG) and silicates (SiO44–) are presented in Table 1.

with ~175 coccospheres per mm2, and a mean separation
between them of ~50 µm. The assemblage was dominatedby Emiliania huxleyi, and we only observed one otherspecimen of H. HOL dalmaticus type and no other Helicosphaera specimens among the 115 coccospheres. So,
the chances of an accidental association were low, and weinterpreted the specimen as providing good evidence of an
actual life-cycle association.
4. Life-cycle interpretation
The holococcolith (H. HOL dalmaticus type) was previously known as S. dalmaticus (Kamptner, 1927) Loeblich& Tappan, 1963. The informal ‘HOL’ terminology usedhere follows the recommendations of Young & Bown
(2014), and reflects the fact that dalmaticus is a form thathas long been assumed to be the haploid stage of a Helicosphaera species because it shows the same distinctive
crystal fabric as the holococcoliths formed by H. carteri
and H. wallichii. Triantaphyllou et al. (2016) published ascanning electron micrograph of a single coccosphere that
had: 1) the same association (pavimentum with dalmaticus); 2) an almost complete coccosphere; and 3) about 50
holococcoliths with three heterococcoliths among these.
That specimen was highly suggestiveof a combination coccosphere, but
because it was a unique specimen,
the authors concluded that further
evidence would be needed before thetaxonomy could be revised. This evidence has been provided by our new
observation, and thus the taxonomy
now requires revision, so that bothphases of the life-cycle have the samename.

3. New observation
During a study of coccolithophore assemblages fromthe central Adriatic Sea, we observed a single, probablecombination coccosphere of the heterococcolith H. pavimentum (Okada & McIntyre, 1977) and the holococcolith
Helicosphaera HOL dalmaticus type. The specimen was acollapsed coccosphere, predominantly formed of about 20
coccoliths of H. pavimentum, with eight coccoliths of H.
HOL dalmaticus type at one end of the coccosphere. Dueto the collapsed nature of the coccosphere, we needed toconsider the possibility that this was an artificial association resulting from two coccospheres coming into chancecontact. The filter had a fairly low density of coccospheres,

Figure 1: Abundance of coccolithophores (cells L-1) in the water column, observed in the SEM,
from Station Stončica, 27 March, 2018

T(°C)
14.05

O2(%)

S
38.52

pH

99.44

8.17

NO3–

NO2–

(µmol L-1)(µmol L-1)

3.151

0.228

NH4+

TIN

NORG

PO43–

PORG

SiO44–(µmol L-1)(µmol L-1)(µmol L-1)(µmol L-1)(µmol L-1)(µmol L-1)

0.079

3.458

5.699

0.0004

0.149

1.781

Table 1: Values of measured environmental parameters

5. Determination of thecorrect name for the
speciesAt first, it appeared that the correct name for the species should be
Syracolithus dalmaticus because thespecies dalmaticus has priority overpavimentum and because it is thetype species of Syracolithus (Kamptner, 1941) Deflandre in Grassé, 1952,
which would have priority over Heli-

Helicosphaera pavimentum life-cycle and Syracolithus dalmaticus taxonomy

cosphaera Kamptner, 1954. This interpretation would involve extensive and undesirable taxonomic revision, andit was clearly preferable to avoid this by making a formal
proposal for the conservation of the name Helicosphaera.
However, a re-examination of the type illustration of
Syracosphaera dalmatica Kamptner, 1927 revealed that itis probably not the same species as the form it has conventionally been used for––Syracolithus dalmaticus (Kamptner, 1927). The type illustration shows coccoliths witha well-defined, narrow spine in the centre of a flat distal
cover with six to eight pores. By contrast, the form thename has been applied to, since the seminal revision of
Kleijne (1991), has a mounded distal surface, with two toseven irregular pores, suggesting that these two coccolithtypes do not belong to the same species. The holococcolith form of the H. pavimentum combination coccosphere
has not otherwise been described, and therefore the only
formal description of the species is actually that of theheterococcolith phase, H. pavimentum, and so no further
nomenclatural revision is needed. The associated heterococcolith and holococcolith phases should be cited using
non-Linnean terminology as H. pavimentum HET and H.
pavimentum HOL.
6. What is the correct identity of
Syracosphaera dalmatica (Kamptner,
1927)?
Having established that the holotype of Syracosphaera
dalmatica does not correspond to the current species concept of Syracolithus dalmaticus, it is then pertinent to ask
which species did Kamptner actually record, especiallybecause this is a rather early illustration of a holococcolithform. Based on the coccolith morphology, there are two
apparent possibilities––the form previously named Zygosphaera wettsteinii Kamptner, 1937, and now referred to
as Syracosphaera mediterranea HOL wettsteinii type, orthe form known as Homozygosphaera vercellii. These twoforms are supposed to have very similar body coccoliths,
but differ in that H. vercellii is monomorphic, whereas
S. mediterranea HOL wettsteinii type is dimorphic (having circumflagellar coccoliths in which the distal surface
flexes upwards to form a transverse bridge). The holotype illustration of S. dalmatica does not show any signof dimorphism, and so is closer to H. vercellii. Hence, S.
dalmatica could be interpreted as a senior synonym of H.
vercellii. This would cause some nomenclatural complica-

43

tions, but not extreme ones. However, H. vercellii and S.
mediterranea HOL wettsteinii type are very similar, so it
is worth asking if they actually represent discrete species.
7. Is the differentiation between
Homozygosphaera vercellii andSyracosphaera mediterranea HOL
wettsteinii type valid?
Zygosphaera wettsteinii was a well-established, widely
recognised species that is now well documented as being aholococcolith morphotype associated with Syracosphaera
mediterranea, based on the observations of Kamptner(1941), Cros et al. (2000) and McGrane (2007). In addition, we have observed multiple specimens of this combination off NW Scotland (JRY, unpubl. data). Two otherholococcolith morphotypes are also associated with S.
mediterranea, which is why this form is referred to as S.
mediterranea HOL wettsteinii type. The other two forms
are S. mediterranea HOL gracillima type and S. mediterranea HOL hellenica type.
Homozygosphaera vercellii, by contrast, is a rare species, which has only occasionally been reported. It is essentially separated from wettsteinii by the absence of
circumflagellar coccoliths. However, on any single coccosphere, there is always the possibility that the circumflagellar coccoliths are simply missing. Moreover, circumflagellar coccoliths are actually present on some of the few
specimens of H. vercellii recorded in the literature, including specimens illustrated by Winter & Siesser (1994) andMalinverno et al. (2008). Young et al. (2003) did suggest
some possible differences in body coccolith morphology
between H. vercellii and Syracosphaera mediterranea
HOL wettsteinii type, but these were very slight. For example, the former bears a smaller central boss and moreangular pores (see also Malinverno et al., 2008), but thesedifferences have proven very difficult to apply. In summary, the vast majority of coccospheres bearing wettsteiniitype holococcoliths are dimorphic, and there seems to be
no justification for treating the specimens without visible
circumflagellar coccoliths as a different species. Hence,
we suggest that H. vercellii is not a discrete species, butrather it and S. dalmaticus are actually S. mediterranea
holococcoliths of the wettsteinii type. Because the terminology S. mediterranea HOL wettsteinii type is informal,
there is no need to rigorously follow priority, and the form
may continue to be referred to as the wettsteinii type.

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Young, Arapov, Skejić, Bakrač, Bužančić, Triantaphyllou

Plate 1

All images at same scale
combination coccosphere of
H. pavimentum and theholococcolith currently
identiﬁed as
H. HOL dalmaticus type

Holotype illustration of S. dalmaticus
Kamptner, 1927––anaccurate representation of
the S. mediterranea
holococcolith phase,
which clearly does notresemble theH. pavimentum
holococcolith phase

Coccospherecurrently identiﬁed as
H. HOL dalmaticus type

Coccosphere of S. mediterranea HOL
wettsteinii type. Note circumﬂagellar
coccoliths (top right)

Helicosphaera pavimentum life-cycle and Syracolithus dalmaticus taxonomy

8. Generic attribution of Coronosphaera
mediterranea vs Syracosphaera
mediterranea
Syracosphaera mediterranea is a formal name, and so thespecies name must follow the rules of nomenclature (Turland et al., 2018). At the species level, this not a problem
because mediterranea has priority over all the other synonymised names.
At the generic level, however, as noted by Triantaphyllou et al. (2016), the inclusion of Zygosphera hellenica in
the life cycle of C. mediterranea made Coronosphaera ajunior synonym of Zygosphaera. The inclusion of Syracolithus dalmaticus (Kamptner, 1927) likewise makes
Syracolithus a senior synonym of Coronosphaera. Triantaphyllou et al. (2016) suggested that, in order to resolve
this problem, the genus Coronosphaera should be abandoned, and any species included in it placed back into Syracosphaera. This recommendation is now unavoidable.
9. Discussion
Among the extant coccolithophores, Syracosphaera is
now the genus with the most species, and contains somerather well-established subgroups (e.g. Cros, 2000; Younget al., 2003; Kleijne & Cros, 2009). However, any possible
formal taxonomic subdivision of the genus that is basedon morphology is liable to be reinterpreted each time newmolecular genetic data becomes available, and any naming of genera split out from Syracosphaera is further liable
to be changed as new life-cycle combinations are found.
For these reasons, we strongly urge the continued useof the genus Syracosphaera in the broad sense, and the
avoidance of assigning generic names to the subgroups.
We would also note that the International Code of Nomenclature (2018) provides mechanisms for conserving
and rejecting names when rigorous application of the principle of priority would cause especially unfortunate namechanges. Moreover, there is one circumstance in which thecode explicitly requires such alternatives to be examined:“Article 57.1 A name that has been widely and persistently
used for a taxon or taxa not including its type is not to be
used in a sense that conflicts with current usage unless anduntil a proposal to deal with it under Art. 14.1 or 56.1 has
been submitted and rejected”.
This is an important, if rarely noted, rule, and it has
been in the Code since at least 1987 (Berlin Code). In thiscase, it could have been argued that, because the name45

Syracolithus has been widely and persistently used for theholococcoliths of Helicosphaera, it should not be redefined to apply to Coronosphaera, even though Syracolithus is a senior synonym of Coronosphaera. In this case,that argument is not worth making because the problem
is avoided by subsuming the genus Coronosphaera into
Syracosphaera, and because it would involve suppressing not one, but two genera (Zygosphaera is also, strictly
speaking, a senior synonym of Coronosphaera). From theperspective of databasing, however, the principle is very
valuable. If the name of a taxon changes (e.g. from Coronosphaera mediterranea to Syracosphaera mediterranea),
this is straightforward to handle. However, if the meaning of a widely-used name is changed, then the result canbe severely deleterious. This principle should be borne inmind when reinterpreting older literature.
Taxonomic appendix
No new formal taxonomy is proposed here, but this list
summarises the recommended terminology for the two
species discussed and their holococcolith stages.
Helicosphaera Kamptner, 1954
Type species: Coccosphaera carteri Wallich, 1877
Helicosphaera pavimentum Okada & McIntyre, 1977
Recommended informal names for the known life-cycle
variants:
Helicosphaera pavimentum HET
Helicosphaera pavimentum HOL
Synonym: Syracolithus dalmaticus (Kamptner, 1927)
auct., non Kamptner (i.e. numerous literature records ofdalmaticus actually represent H. pavimentum holococcoliths, but these do not include the type specimen).
Syracosphaera Lohmann, 1902
Type species: Syracosphaera pulchra Lohmann, 1902
Synonyms:
Syracolithus (Kamptner, 1941) Deflandre in Grassé, 1952
– type species S. dalmaticus
Coronosphaera Gaarder in Gaarder & Heimdal, 1977 –type species C. mediterranea
Zygosphaera Kamptner, 1936 – type species Z. hellenica
Kamptner, 1937, designated by Loeblich & Tappan, 1963
See Nannotax3 (http://ina.tmsoc.org/Nannotax3/index.
html) for an extended synonymy.

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Young, Arapov, Skejić, Bakrač, Bužančić, Triantaphyllou

Syracosphaera mediterranea Lohmann, 1902
Synonyms:
Coronosphaera mediterranea (Lohmann, 1902) Gaarderin Gaarder & Heimdal, 1977
Syracosphaera dalmatica Kamptner, 1927
Homozygosphaera vercellii Borsetti & Cati, 1979
Syracolithus dalmaticus (Kamptner, 1927) Kleijne, 1991
See Triantaphyllou et al. (2016) for an extended synonymy.
Recommended informal names for the known life-cycle
variants:
Syracosphaera mediterranea HET
Syracosphaera mediterranea HOL gracillima type
Syracosphaera mediterranea HOL hellenica type
Syracosphaera mediterranea HOL wettsteinii type
Acknowledgements
This work was supported, in part, by the Croatian Science Foundation under project IP-2014-09-3606.

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